Genetic Variability of Passiflora Spp. Against Collar Rot Disease

AJCS 9(1):69-74 (2015) ISSN:1835-2707

Genetic variability of Passiflora spp. against collar rot disease

Sandra da Costa Preisigke*1, Felipe Vian Martini2, Ana Aparecida Bandini Rossi3, Milson Evaldo Serafim4, Marco Antonio Aparecido Barelli2, Petterson Baptista da Luz2, Kelly Lana Araújo2, Leonarda Grillo Neves2

1University of Norte Fluminense Darcy Ribeiro, Brazil 2University of the State of Mato Grosso, Brazil, Department of Agronomy, Brazil 3University of the State of Mato Grosso, Department of Biological Sciences, Brazil 4Federal Institute of Education, Science and Technology of Mato Grosso, Brazil

*Corresponding author: [email protected]

Abstract

Collar rot caused by the fungus Fusarium solani, is one of the main diseases in passion fruit orchards. Some disease resistance sources were previously identified in wild species of Passiflora; however, information is limited and contradictory concerning disease resistance within Passiflora species. The objective of this study was to evaluate intra and interspecific variability of ten Passiflora species regarding to their resistance characters against Fusarium solani. Cuttings (clones) form four different genotypes from the ten species studied were prepared, with a total of 40 genotypes. Resistance or susceptibility was evaluated by the plant survival period and by a disease assessment scale. Data was analyzed using variance analysis, test of means, graphical dispersion and the hierarchical clustering method UPGMA. Intra and interspecific variability of resistance against F. solani was confirmed, being P. quadrangularis, P. nítida and P. foetida evaluated as highly resistant. The most suitable species for plant breeding programs is P. nitida, since it showed a high resistance level without genetic variability within the characters studied.

Keywords: Genetic resistance. Fusarium solani. Passion fruit. Cutting. Plant Breeding. Abbreviations: t_ tonelada; UNEMAT_Universidade do Estado de Mato Grosso; UFV Universidade Federal de Viçosa; UENF_Universidade Estadual do Norte Fluminense Darcy Ribeiro; km_kilometer; BAG_ germpalsm active bank; BDA_potato, dextrose, agar; B.O.D_biochemical oxygen demand; PVC_ polyvinyl chloride; mm_ millimeter; DAI_ days after inoculation; NS_Note scale; PS_Survival period; UPGMA_unweighted pair group method with arithmetic mean; SQM_mean square residue.

Introduction

Yellow passion fruit (Passiflora edulis Sims) belongs to the however, recent studies have demonstrated that F. solani f. Genera Passiflora, the biggest and most important within the sp. passiflorae is an specialized form that infects yellow family Passifloraceae, it is original from the tropical and passion fruit (Bueno et al., 2014). Symptoms of the disease subtropical America (Vanderplank, 2000) and widely consist of a light apical wilt followed by color alterations of cultivated in countries like Brazil, Ecuador, Venezuela, leaves and a subsequently severe wilt, defoliation and death, Colombia and other countries outside America as South as a result of a complete necrosis of the collar region. Africa, Kenya, Zimbabwe, India and New Zealand Necrosis extents 2-10 cm above the soil and in some cases it (Vanderplank, 1996; Manicom et al., 2003). Brazil has a vast advances to the roots (Bueno et al., 2014). The pathogen diversity of passion fruit species with about 141species develops resistance structures, the chlamydospores that already known (Bernacci et al., 2014). Brazil is considered remain in the soil for several years, even in the absence of the one of the biggest world producing countries and the biggest host plant (Fischer et al., 2005a). Due to these characteristics producer of yellow passion fruit (FAO, 2014). However, in collar rot is a difficult disease to control. In passion fruit 2012 a reduction of approximately 16% production was orchards the disease incidence results in a significant verified when compared to 2011, with a production of reduction of productivity, need of constant migration or scape 776.097 t in 2012 contrasting with a 923.035 t in 2011. The to new areas free from the pathogen and reduction of the reduction in passion fruit production is related primarily with orchard’s lifespan. The development of an effective strategy the incidence of diseases (Cavichioli et al., 2011). Amongst to control collar rot disease is still at preliminary stage (or the main plant disease problems contributing for the low experimental), as for example biological control using productivity of passion fruit orchards in Brazil, basal or collar Trichoderma spp. and chemical products (Meza et al., 2008; rot has a leading role (Viana and Costa 2003; Fischer al., Fischer et al., 2010b; Silva et al., 2014). Disease control 2005a), caused by the fungus Fusarium solani, the imperfect using rootstocks has been also studied. Junqueira et al. (2006) form of Haematonectria haematococca (Berkeley & verified that commercial passion fruit grafted with P. nitida Broome) Samuels & Nirenberg (Leslie & Summerell 2006). shows good performance in areas previously affected by the This is a polyphagous fungus affecting a wide number of disease. In the study performed by Fischer et al. (2010b), also cultivated plants as peanut (Casasnovas et al., 2013), tomato evaluating rootstocks, they concluded that the species P. (Castaño et al., 2012), beans (Sasan et al., 2013), etc, maliformis, P. suberosa and P. alata are resistant to collar

Table 1. Summary of analysis of variance of genetic resistance of 10 species of Passiflora about the F. solani. SQM2 Source of variation G.L1 EN PS Blocks 3 0.74 62.58 Species 9 6.57 ** 524.19** Waste 27 0.82 100.65 Average 4.72 31.55 C.V (%) 19.21 31.80 (**) Significant at 1% by test F; 1G.L_degree of freedom; 2SQM_ mean square residue; EN_assessment scale and PS_survival period.

Fig 1. Graphical dispersion of measurements obtained in the assessments of rating scale and survival period (average of 4 plants) in relation to the behavior of 10 species of Passiflora to Fusarium solani. Species are represented by the numbers: 1- P. quadrangularis; 2- P. nitida; 3- P. foetida; 4- P. eichleriana; 5- P. alata, 6- P. cincinnata; 7- P. mucronata, 8- P. suberosa; P. morifolia e 10- P. edulis. rot. Considering the significance of the yellow passion fruit mean values in the disease assessment scale (Table 2). Thus, cultivation in Brazil, as well as the importance of the disease these were the most susceptible species against the pathogen. caused by F. solani, the lack of more efficient control On the other hand, the species P. nitida and P. foetida had the strategies and the need for exploiting the genetic diversity of higher survival period, all plants survived 50 evaluation days the Passiflora species that can reveal sources of resistance, and had the lowest mean values or the disease assessment this work was developed with the aim to: 1) find one resistant scale. The species were gathered according to the means species against the fungus F. solani within the Genera observed for both resistance characters by the method of Passiflora, 2) evaluate the existence of genetic variability distance projection 2D (Fig. 1), these results confirm the concerning resistance against the pathogen within the species. previously ones showed above. It was possible to observe the formation of four clusters with different levels of resistance. Results P. nitida (2) and P. foetida (3), included within the same cluster, were e the most resistant against the pathogen, Detection of resistant species (interspecific variability) followed by P. quadrangularis (1). In contrast, P. mucronata (7) was the most susceptible to the fungus. The majority of Significant differences were observed for all characteristics the species formed a cluster of plants considered susceptible, evaluated (Table 1), thus indicating the possibility of since the mean values for the period of survival character selection of resistant species against collar rot, either for were low while the ones for the disease assessment scale developing plant breeding programs or for their use as were high. This cluster comprehends the species P. alata, P. rootstock plants. Plant death was observed five days after eichleriana, P. edulis, P. cincinnata, P. suberosa, P. inoculation (DAI) in P. mucronata, P. morifolia, P. suberosa, morifolia. In a study performed by Fischer et al., (2005b), P. cincinnata, P. alata and P. eichleriana. These species had they also verified susceptibility of the species P. cincinnata, the lowest mean values for the survival period and the highest P. suberosa and P. edulis.

Table 2. Assessment scale assigned to the symptoms of collar rot and period of survival of the species of Passiflora in 50 days of ratings. Resistance characteristics 1 Species EN PS P. quadrangularis 3.58 bcd2 40.58 ab P. nitida 2.33 d 50.0 a P. foetida 2.92 cd 50.0 a P. eichleriana 5.58 ab 30.5 ab P. alata 4.92 abc 28.42 ab P. cincinnata 5.5 ab 25.0 b P. mucronata 5.92 a 17.92 b P. suberosa 5.5 ab 22.92 b P. morifolia 5.5 ab 22.0 b P. edulis 5.42 ab 28.17 ab 1 Averages of four plants (repetitions). 2 Means followed by the same letter in the column do not differ (Tukey, p<0,05); EN_assessment scale and PS_survival period.

Fig 2. Dendrogram the resulting analysis of 40 genotypes of Passiflora based on two features of resistance to the fungus F. solani obtained by the UPGMA clustering method, using Mahalanobis distance as a measure of the genetic distance. Where the 1-4 are the species P. quadrangularis; 5 a 8 P. nitida; 9 a 12 P. foetida; 13 a 16 P. eichleriana; 17 a 20 P. alata; 21 a 24 P. cincinnata; 25 a 28 P. mucronata; 29 a 32 P. suberosa; 33 a 36 P. morifolia e 37 a 40 P. edulis.

Genetic diversity of 40 genotypes of Passiflora based in against collar rot within the species studied. With a split-up at characteristics of resistance against F. solani. number 15 it is possible to observe the formation of four clusters with different degrees of resistance against the From a total of 360 plants, 153 wilted and died. The pathogen pathogen. The first group was formed with 52.5% of was re-isolated from some of those plants to confirm the genotypes with three genotypes of species P. edulis (38, 39 cause of death. The cophenetic correlation coefficient and 37), one P. alata (20), four P. mucronata (26, 25, 27 and obtained between the generalized distance of Mahalanobis 28), three P. suberosa (30, 29 and 32), three P. morifolia (36, (D2) matrix and the cophenetic distance (C) matrix was of 34 and 35), three P. eichleriana (14, 16 and 13), four P. 0.80, thus revealing a good correlation between the graphic cincinnata (21, 22, 23 and 24), one P. quadrangularis (1), representation of the distances and its original matrix (Rohlf, according to the order of numbers represented in Fig. 2. 2000), allowing to achieve inferences by means of a visual These genotypes showed high susceptibility degree, once the evaluation of the Fig. 2. Based on the arrangement in mean values for the maximum survival period was of 35 days different clusters by the UPGM method (Fig.2) it is possible and the lowest assessment scale value was 5. to confirm that there is genetic variability for resistance 71

Table 3. Representation of four distinct genotypes of each species, a total of 40 genotypes (treatment) evaluated. Genotypes Species Genotypes Species Genotypes Species Genotypes Species 1 P.quadrangularis 11 P. foetida 21 P. cincinnata 31 P.suberosa 2 P.quadrangularis 12 P. foetida 22 P. cincinnata 32 P.suberosa 3 P.quadrangularis 13 P.eichleriana 23 P. cincinnata 33 P.morifolia 4 P.quadrangularis 14 P.eichleriana 24 P. cincinnata 34 P.morifolia 5 P. nitida 15 P.eichleriana 25 P.mucronata 35 P.morifolia 6 P. nitida 16 P.eichleriana 26 P.mucronata 36 P.morifolia 7 P. nitida 17 P. alata 27 P. mucronata 37 P. edulis 8 P. nitida 18 P. alata 28 P. mucronata 38 P. edulis 9 P. foetida 19 P. alata 29 P. suberosa 39 P. edulis 10 P. foetida 20 P. alata 30 P. suberosa 40 P. edulis

The second cluster was constituted only 15% of the studies had also demonstrated the resistance of P. nitida genotypes with one genotype of specie P. suberosa (31), one against soilborne pathogens (Fischer et al., 2005b; Junqueira P. morifolia (33), three P. alata (17, 19 and 18), one P. et al., 2010). According to these authors, P. nitida, in addition quadrangularis (4) and one P. edulis (40). These genotypes to be rustic, possesses significant resistance against the showed a higher degree of resistance when compared with disease and has potential to be used in breeding programs that the previous cluster, once the mean value for the maximum will include interspecific hybridization. High levels of period of survival was of 40 days. The constitution of these genetic variability were observed within the genotypes, even two clusters evidences the genetic diversity of the genotypes when belonging to the same species. Bueno et al. (2014), regarding resistance against F. solani, once there were while characterizing a F. solani population, identified isolates genotypes of the same species gathered in both clusters, as with different levels of aggressivity on yellow passion fruit, for example P. alata. The third cluster was formed with the the authors attributed such differences to the variability lowest number of genotypes, only 7.5%, constituted by the within the species or variability of the pathogen. In the species P. foetida (genotypes 9 and 11) and P. eichleriana present study, variability is derived only from the genotypes (genotype 15). Genotypes of this group showed moderated studied, with inocula being originated from a single spore resistance against the pathogen due to the survival of all (monosporic). This variation in Passiflora resistance, genotypes during 50 evaluation days, but having relatively pathogen aggressivity and its significant interactions must be high mean values for the disease assessment scale, of considered when developing breeding programs. In previous approximately 5. The last cluster was formed by 20% of the studies accomplished by Silva et al. (2013) to characterize genotypes, constituted by the species P. quadrangularis resistant passifloras against Fusarium oxysporum f. sp. (genotypes 2 and 3), P. nitida (genotypes 7, 5, 6 and 8) and Passiflorae, resistance variability of genotypes of the same P. foetida (genotypes 10 and 12). Plants within this group species was also observed. These results reveal that resistance were considered highly resistant once the mean value for the probably depends of the genotype. The genotypes form the P. survival period was of 50 days and the disease assessment edulis species studied were considered susceptible and having scale value ranged from 1 to 2,6. The species showing the variability in their resistance degree, as previously observed higher variation of resistance was P. quadrangularis. by Fisher et al. (2010a), when besides detecting susceptibility Genotypes of this species are present within three clusters, against an isolate of F. solani in the yellow passion fruit from the most susceptible to the most resistant. In contrast, variety Afruvec, they detected high variability in the resistant genotypes form the species P. nitida had no variation in reaction in different genotypes of yellow passion fruit. resistance degree, besides being the species with the best Further studies (Cavichioli et al., 2011; Meza et al., 2008) performance. also detected that genotypes of these species had no resistance against collar rot disease. This results show the Discussion need to incorporate genes of resistance into the commercial species (P. edulis), found in wild species, by means of classic In this work the species P. mucronata showed the highest methods of plant breeding. Differences in resistance between susceptibility to the pathogen. Previous work by Fischer et al. and within each genotype may be associated with the high (2010b) confirms this result, when P. mucronata used as a level of heterozygosity of the Passiflora species, therefore rootstock was evaluated as susceptible against the pathogen. justifying the selection of intraspecific resistant species. This In a study performed by Fischer et al. (2005b), evaluating diversity must be considered in plant breeding programs different species within the Genera Passiflora against F. aiming resistant cultivars against the collar rot disease, being solani, the authors confirmed species P. nitida and P. alata as of substantial importance to include an evaluation for intra resistant and P. cicinnata as susceptible, matching results and interspecific resistance in the germplasm observed in the present study except for P. alata, evaluated as characterization. The species P. nitida had no variability susceptible in the present study. Contradictory results to the against collar rot disease, once all the genotypes of the present study were observed by Fischer et al. (2010b), where species evaluated were grouped as resistant, as observed in these authors observed found P. alata and P. suberosa previous studies (Fischer et al., 2005b; Roncatto et al, 2004). species, as being resistant against collar rot disease when This species showed resistance to the pathogen, therefore is used as rootstocks. When comparing different studies, the most fitted to be used in breeding programs targeting the contrasting results are observed, this variation may be transference of resistance genes against F. solani to the associated to a genetic diversity within the species resistance commercial P. edulis species. against the fungus. The species P. quadrangularis, P. nitida and P. foetida were evaluated as the most resistant. Some 72

Materials and Methods using a scale ranging from 1 to 6, being 1= absence of symptoms; 2= light symptoms: necrosis in just a part of the Experimental area plant, less than 50% of the stem circumference; 3= moderate symptoms: necrosis in more than 50% of the stem The experiment was performed at the experimental area of circumference, with destruction of the cortex but without the Universidad of Estate de Mato Grosso (UNEMAT), destruction of the plant medulla; 4= moderate symptoms: Campus Cáceres, located in the Southwest region of the Mato with a less extent of the cortex necrosis but with extended Grosso state, Brazil, latitudes 15º 27’ and 17º 37’ South and necrosis of the medulla; 5= severe symptoms: extensive longitudes 57º 00’ and 58º 48’ West, at an altitude of 118 m colonization of the stem and necrosis of the medulla and above the sea level. The county is part of the middle-region cortex; 6= dead plant. of the Center-South State of Mato Groso and the Alto

Pantanal micro-region, at a distance of 215 km from the Statistical analysis capital, with a tropical hot and humid climate and a dry winter (Neves et al., 2011). Initially, data of resistance characters (disease assessment

scale and survival period) were submitted to variance Implementation of the working collection and preparation analysis in order to verify genetic variability between the ten of cuttings species studied, then, the mean values were compared by Tukey’s test at 5% probability. Means were also grouped The implementation of the Passiflora working collection at according the methodology of Graphical Dispersion UNEMAT was accomplished by the planting of 10 species in Projection 2D. In order to reveal the intraspecific genetic field conditions: P. nitida, P. alata, P. mucronata, P. variability of the resistance within Passiflora species, the 40 cincinnata, P. morifolia, P. suberosa, P. foetida, P. genotypes were distinguished by the UPGMA hierarchical eichleriana, P. quadrangularis, and one genotype of the clustering method, using as dissimilarity measure the average commercial species P. edulis derived from the breeding 2 Mahalanobis distance (D ) and the correction between program from UFV/UNEMAT/UENF. All the seeds used distances’ matrix and the dendrogram were estimated by the were originated from the Active Germplasm Bank (BAG) cophenetic correlation coefficient (ccc). All analysis was from UNEMAT. After the establishment of the plants in the performed with the aid of the software Genes® (Cruz, 2013). field, cuttings containing two or three buds were made from the median portion of vegetative branches. In order to Conclusions evaluate the variability within the 10 species under study, four cuttings of different plants were prepared, with a total of Intra and interspecific variability of resistance against 40 genotypes that were identified by a number, as shown in Fusarium solani do exists within the studied Passiflora Table 3. Cuttings were rooted in trays of 72 cells distributed species. Species P. nitida, P. foetida and P. quadragularis in random block design with 40 treatments (genotypes), three had the highest resistance level. The most adequate species replicates and three plants per parcel, with a total of 360 for plant breeding programs of passion fruit aiming resistance plants evaluated. against F. solani is P. nitida, once those genotypes showed

no variation in resistance. Isolate preparation and inoculation of Fusarium solani

Acknowledgments After rooting, cuttings were inoculated with the fungus

Fusarium solani. To avoid interference of genetic variability To the University of the State of Mato Grossso, the team of of the fungus, the monosporic isolate FS04, from the the Plant Breeding Laboratory and the research institutions, mycology collection at the Laboratory of Genetic Breeding – the Foundation for Research Hosting of the Mato Grosso UNEMAT, was used for inoculation. For the inoculum State (FAPEMAT) and Coordination of Improvement of preparation, monosporic isolate FS04, preserved in filter Higher Level (CAPES). paper, was replicated in Petri dishes containing BDA and incubated in growing chamber (B.O.D.) at 24 oC and light References period of 12 h during 7 days. Inoculation was performed as described by Fischer et al. (2003). A discus (5 mm diameter) Bernacci LC, Cervi AC, Milward-de-Azevedo MA, Nunes of culture media containing profuse mycelium growth was TS, Imig DC, Mezzonato AC (2014) Passifloraceae. In: retired from the Petri dishes and fixed with PVC plastic tape Lista de espécies da flora do Brasil. Jardim botânico do Rio over a small injury in the plant stem, at a distance of 2 cm de Janeiro. Available online at http://www.floradobrasil. from the soil. The plastic tape was removed five days after jbrj.gov.br/jabot/ floradobrasil/FB12506. (Accessed on inoculation (DAI). The same procedure was applied to the April, 2014). control treatment, but without the media culture discus Bueno CJ, Fischer IH, Rosac DD, Firminod AC, Harakavae containing fungus. R, Oliveira CMG, Furtado EL (2014) Plant Pathology Fusarium solani f. sp. passiflorae: a new forma specialis Disease evaluation causing collar rot in yellow passion fruit. Plant Pathol. 63:382–389. The response of the inoculated plants were analyzed by Casasnovas F, Fantini EN, Palazzini JM, Giaj-Merlera G, means of: i- the survival period, considered as the number of Chulze SN, Reynoso MM, Torres AM (2013) days elapsed from the inoculation until the plant death or Development of amplified fragment length polymorphism until 50 days of evaluation and ii- through a disease (AFLP)-derived specific primer for the detection of assessment scale, modified from Roy (1997). The disease assessment scale was applied in the last day of evaluation, 73

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